High-throughput direct fecal PCR assay for detection of Mycobacterium avium subsp. Paratuberculosis in sheep and cattle

Journal of Clinical Microbiology

Volumn 52, Issue 3, 2014, Pages 745-757

  Plain, Karren M ^a   Marsh, Ian B ^b   Waldron, Anna M ^a   Galea, Francesca ^b   Whittington, Ann Michele ^a   Saunders, Vanessa F ^b   Begg, Douglas J ^a   De Silva, Kumudika ^a   Purdie, Auriol C ^a   Whittington, Richard J ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b NSW DEPARTMENT OF PRIMARY INDUSTRIES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; CELL DNA; GENOMIC DNA;

ARTICLE; BACTERIAL CELL; BACTERIAL COUNT; BACTERIUM CULTURE; BACTERIUM DETECTION; BACTERIUM ISOLATE; CATTLE DISEASE; CLINICAL PROTOCOL; CONSENSUS; CONTROLLED STUDY; DAIRY CATTLE; DIAGNOSTIC TEST ACCURACY STUDY; DNA EXTRACTION; DNA SEQUENCE; FECES ANALYSIS; FECES CULTURE; FEMALE; GOLD STANDARD; HIGH THROUGHPUT JOHNES TEST; HIGH THROUGHPUT SCREENING; LIMIT OF DETECTION; LIMIT OF QUANTITATION; LIQUID CULTURE; MALE; MCNEMAR TEST; MYCOBACTERIUM PARATUBERCULOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRACTICE GUIDELINE; PRIORITY JOURNAL; QUANTITATIVE DIAGNOSIS; RADIOMETRY; SAMPLING; SENSITIVITY AND SPECIFICITY; SHEEP DISEASE; SUSPENSION; VALIDATION STUDY;

ANIMALS; AUSTRALIA; BACTERIOLOGICAL TECHNIQUES; CATTLE; CATTLE DISEASES; FECES; MOLECULAR DIAGNOSTIC TECHNIQUES; MYCOBACTERIUM AVIUM SUBSP. PARATUBERCULOSIS; NEW ZEALAND; PARATUBERCULOSIS; REAL-TIME POLYMERASE CHAIN REACTION; SHEEP; SHEEP DISEASES; VETERINARY MEDICINE;

EID: 84894556854     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.03233-13     Document Type: Article

References (43)

1. Nielsen SS, Toft N, Gardner IA. 2011. Structured approach to design of diagnostic test evaluation studies for chronic progressive infections in animals. Vet. Microbiol. 150:115-125. http://dx.doi.org/10.1016/j.vetmic .2011.01.019.
2. Gardner IA, Nielsen SS, Whittington RJ, Collins MT, Bakker D, Harris B, Sreevatsan S, Lombard JE, Sweeney R, Smith DR, Gavalchin J, Eda S. 2011. Consensus-based reporting standards for diagnostic test accuracy studies for paratuberculosis in ruminants. Prev. Vet. Med. 101:18-34. http://dx.doi.org/10. 1016/j.prevetmed.2011.04.002.
3. Whittington RJ, Begg DJ, de Silva K, Plain KM, Purdie AC. 2012. Comparative immunological and microbiological aspects of paratuberculosis as a model mycobacterial infection. Vet. Immunol. Immunopathol. 148:29-47. http://dx.doi.org/10.1016/j.vetimm.2011.03.003.
4. Whittington RJ, Whittington AM, Waldron A, Begg DJ, de Silva K, Purdie AC, Plain KM. 2013. Development and validation of a liquid medium (M7H9C) for routine culture of Mycobacterium avium subsp. Paratuberculosis to replace modified Bactec 12B medium. J. Clin. Microbiol. 51:3993-4000. http://dx.doi.org/10.1128/JCM.01373-13.
5. Sibley JA, Woodbury MR, Appleyard GD, Elkin B. 2007. Mycobacterium avium subspecies paratuberculosis in bison (Bison bison) from northern Canada. J. Wildl. Dis. 43:775-779. http://dx.doi.org/10.7589/0090-3558 -43.4.775. (Pubitemid 350162456)
6. Forde T, De Buck J, Elkin B, Kutz S, van der Meer F, Orsel K. 2013. Contrasting results of culture-dependent and molecular analyses of Mycobacterium avium subsp. Paratuberculosis from wood bison. Appl. Environ. Microbiol. 79:4448-4454. http://dx.doi.org/10.1128/AEM.00995-13.
7. Whittington RJ. 2009. Factors affecting isolation and identification of Mycobacterium avium subsp. Paratuberculosis from fecal and tissue samples in a liquid culture system. J. Clin. Microbiol. 47:614-622. http://dx .doi.org/10.1128/JCM.01986-08.
8. Whittington RJ. 2010. Cultivation of Mycobacterium avium subsp. Paratuberculosis, p 244-266. In Behr MA, Collins DM (ed), Paratuberculosis: organism, disease, control. CABI, Wallingford, United Kingdom.
9. Monteiro L, Bonnemaison D, Vekris A, Petry KG, Bonnet J, Vidal R, Cabrita J, Mégraud F. 1997. Complex polysaccharides as PCR inhibitors in feces: Helicobacter pylori model. J. Clin. Microbiol. 35:995-998. (Pubitemid 27146555)
10. Thornton CG, Passen S. 2004. Inhibition of PCR amplification by phytic acid, and treatment of bovine fecal specimens with phytase to reduce inhibition. J. Microbiol. Methods 59:43-52. http://dx.doi.org/10.1016/j .mimet.2004.06.001. (Pubitemid 39119912)
11. Kreader CA. 1996. Relief of amplification inhibition in PCR with bovine serum albumin or T4 gene 32 protein. Appl. Environ. Microbiol. 62:1102- 1106. (Pubitemid 26071491)
12. Whittington RJ, Sergeant ES. 2001. Progress towards understanding the spread, detection and control of Mycobacterium avium subsp. Paratuberculosis in animal populations. Aust. Vet. J. 79:267-278. http://dx.doi.org /10.1111/j.1751-0813.2001.tb11980.x. (Pubitemid 33644859)
13. Bull TJ, McMinn EJ, Sidi-Boumedine K, Skull A, Durkin D, Neild P, Rhodes G, Pickup R, Hermon-Taylor J. 2003. Detection and verification of Mycobacterium avium subsp. Paratuberculosis in fresh ileocolonic mucosal biopsy specimens from individuals with and without Crohn's disease. J. Clin. Microbiol. 41:2915-2923. http://dx.doi.org/10.1128/JCM.41 .7.2915-2923.2003. (Pubitemid 36842279)
14. Kawaji S, Taylor DL, Mori Y, Whittington RJ. 2007. Detection of Mycobacterium avium subsp. Paratuberculosis in ovine faeces by direct quantitative PCR has similar or greater sensitivity compared to radiometric culture. Vet. Microbiol. 125:36-48. http://dx.doi.org/10.1016/j.vetmic .2007.05.002. (Pubitemid 47446056)
15. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT. 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55:611-622. http://dx.doi.org/10.1373/clinchem.2008. 112797.
16. Begg D, Whittington R. 2010. Paratuberculosis in sheep, p 157-168. In Behr MA, Collins DM (ed), Paratuberculosis: organism, disease, control. CABI Wallingford, United Kingdom.
17. Marsh IB, Bannantine JP, Paustian ML, Tizard ML, Kapur V, Whittington RJ. 2006. Genomic comparison of Mycobacterium avium subsp. Paratuberculosis sheep and cattle strains by microarray hybridization. J. Bacteriol. 188:2290-2293. http://dx.doi.org/10.1128/JB.188.6.2290-2293 .2006. (Pubitemid 43376484)
18. Whittington RJ, Marsh I, McAllister S, Turner MJ, Marshall DJ, Fraser CA. 1999. Evaluation of modified Bactec 12B radiometric medium and solid media for culture of Mycobacterium avium subsp. Paratuberculosis from sheep. J. Clin. Microbiol. 37:1077-1083. (Pubitemid 29140617)
19. Whittington RJ, Marsh I, Turner MJ, McAllister S, Choy E, Eamens GJ, Marshall DJ, Ottaway S. 1998. Rapid detection of Mycobacterium paratuberculosis in clinical samples from ruminants and in spiked environmental samples by modified Bactec 12B radiometric culture and direct confirmation by IS900 PCR. J. Clin. Microbiol. 36:701-707. (Pubitemid 28093253)
20. Reddacliff LA, Nicholls PJ, Vadali A, Whittington RJ. 2003. Use of growth indices from radiometric culture for quantification of sheep strains of Mycobacterium avium subsp. Paratuberculosis. Appl. Environ. Microbiol. 69:3510-3516. http://dx.doi.org/10.1128/AEM.69.6.3510 -3516.2003. (Pubitemid 36693361)
21. Plain KM, Purdie AC, Begg DJ, de Silva K, Whittington RJ. 2010. Toll-like receptor (TLR)6 and TLR1 differentiation in gene expression studies of Johne's disease. Vet. Immunol. Immunopathol. 137:142-148. http://dx.doi.org/10.1016/j. vetimm.2010.04.002.
22. Begg DJ, de Silva K, Di Fiore L, Taylor DL, Bower K, Zhong L, Kawaji S, Emery D, Whittington RJ. 2010. Experimental infection model for Johne's disease using a lyophilised, pure culture, seedstock of Mycobacterium avium subspecies paratuberculosis. Vet. Microbiol. 141:301-311. http://dx.doi.org/10.1016/j. vetmic.2009.09.007.
23. Purdie AC, Plain KM, Begg DJ, de Silva K, Whittington RJ. 2012. Expression of genes associated with the antigen presentation and processing pathway are consistently regulated in early Mycobacterium avium subsp. Paratuberculosis infection. Comp. Immunol. Microbiol. Infect. Dis. 35:151-162. http://dx.doi.org/10.1016/j.cimid.2011.12.007.
24. Animal Health Australia. 2013. Bovine Johne's disease in Australia. Animal Health Australia, Deakin, Australian Capital Territory, Australia. http://www.animalhealthaustralia.com.au/programs/johnes-disease/ bovine-johnes-disease-in-australia/.
25. Dhand NK, Johnson WO, Eppleston J, Whittington RJ, Windsor PA. 2013. Comparison of pre- and post-vaccination ovine Johne's disease prevalence using a Bayesian approach. Prev. Vet. Med. 111:81-91. http://dx.doi.org/10.1016/j. prevetmed.2013.03.003.
26. McGregor H, Dhand NK, Dhungyel OP, Whittington RJ. 2012. Transmission of Mycobacterium avium subsp. Paratuberculosis: dose-response and age-based susceptibility in a sheep model. Prev. Vet. Med. 107:76-84. http://dx.doi.org/ 10.1016/j.prevetmed.2012.05.014.
27. Petrie A, Watson P. 2006. Statistics for veterinary and animal science, 2nd ed. Blackwell Publishing, Oxford, United Kingdom.
28. Motulsky H. 1995. Intuitive biostatistics: a nonmathematical guide to statistical thinking. Oxford University Press, Oxford, United Kingdom.
29. World Organisation for Animal Health (OIE). 2013. Chapter 1.1.5: principles and methods of validation of diagnostic assays for infectious diseases. In Manual of diagnostic tests and vaccines for terrestrial animals. OIE, Paris, France.
30. Caraguel CG, Stryhn H, Gagné N, Dohoo IR, Hammell KL. 2011. Selection of a cutoff value for real-time polymerase chain reaction results to fit a diagnostic purpose: analytical and epidemiologic approaches. J. Vet. Diagn. Invest. 23:2-15. http://dx.doi.org/10.1177 /104063871102300102.
31. Leite FL, Stokes KD, Robbe-Austerman S, Stabel Jr. 2013. Comparison of fecal DNA extraction kits for the detection of Mycobacterium avium subsp. Paratuberculosis by polymerase chain reaction. J. Vet. Diagn. Invest. 25:27-34. http://dx.doi.org/10.1177/1040638712466395.
32. Petrich A, Mahony J, Chong S, Broukhanski G, Gharabaghi F, Johnson G, Louie L, Luinstra K, Willey B, Akhaven P, Chui L, Jamieson F, Louie M, Mazzulli T, Tellier R, Smieja M, Cai W, Chernesky M, Richardson SE, Ontario Laboratory Working Group for the Rapid Diagnosis of Emerging Infections. 2006. Multicenter comparison of nucleic acid extraction methods for detection of severe acute respiratory syndrome coronavirus RNA in stool specimens. J. Clin. Microbiol. 44:2681-2688. http://dx.doi.org/10.1128/JCM.02460-05. (Pubitemid 44228557)
33. Fang X, Willis RC, Burrell A, Evans K, Hoang Q, Xu W, Bounpheng M. 2007. Automation of nucleic acid isolation on KingFisher magnetic particle processors. J. Lab. Autom. 12:195-201. http://dx.doi.org/10.1016/j.jala .2007.05.001. (Pubitemid 47046753)
34. Kim S, Park SJ, Namgoong S, Sung H, Kim MN. 2009. Comparative evaluation of two automated systems for nucleic acid extraction of BK virus: NucliSens easyMAG versus BioRobot MDx. J. Virol. Methods 162: 208-212. http://dx.doi.org/10.1016/j.jviromet.2009.08.007.
35. Green EP, Tizard ML, Moss MT, Thompson J, Winterbourne DJ, McFadden JJ, Hermon-Taylor J. 1989. Sequence and characteristics of IS900, an insertion element identified in a human Crohn's disease isolate of Mycobacterium paratuberculosis. Nucleic Acids Res. 17:9063-9073. http://dx.doi.org/10.1093/ nar/17.22.9063. (Pubitemid 20003172)
36. Cousins DV, Whittington R, Marsh I, Masters A, Evans RJ, Kluver P. 1999. Mycobacteria distenct [sic] from Mycobacterium avium subsp. Paratuberculosis isolated from the faeces of ruminants possess IS900-like sequences detectable by IS900 polymerase chain reaction: Implications for diagnosis. Mol. Cell Probes 13:431-442. http://dx.doi.org/10.1006/mcpr .1999.0275. (Pubitemid 30088436)
37. Taddei R, Barbieri I, Pacciarini ML, Fallacara F, Belletti GL, Arrigoni N. 2008. Mycobacterium porcinum strains isolated from bovine bulk milk: implications for Mycobacterium avium subsp. Paratuberculosis detection by PCR and culture. Vet. Microbiol. 130:338-347. http://dx.doi.org/10 .1016/j.vetmic.2008.02.007.
38. Englund S, Bölske G, Johansson KE. 2002. An IS900-like sequence found in a Mycobacterium sp. other than Mycobacterium avium subsp. Paratuberculosis. FEMS Microbiol. Lett. 209:267-271. http://dx.doi.org/10.1111 /j.1574-6968.2002.tb11142.x. (Pubitemid 34465603)
39. Cook KL, Britt JS. 2007. Optimization of methods for detecting Mycobacterium avium subsp. Paratuberculosis in environmental samples using quantitative, real-time PCR. J. Microbiol. Methods 69:154-160. http://dx .doi.org/10.1016/j.mimet.2006.12.017. (Pubitemid 46427936)
40. Möbius P, Hotzel H, Rassbach A, Köhler H. 2008. Comparison of 13 single-round and nested PCR assays targeting IS900, ISMav2, f57 and locus 255 for detection of Mycobacterium avium subsp. Paratuberculosis. Vet. Microbiol. 126:324-333. http://dx.doi.org/10.1016/j.vetmic.2007.07 .016. (Pubitemid 350192087)
41. Castellanos E, de Juan L, Domínguez L, Aranaz A. 2011. Progress in molecular typing of Mycobacterium avium subspecies paratuberculosis. Res. Vet. Sci. 92:169-179. http://dx.doi.org/10.1016/j.rvsc.2011.05.017.
42. Wells SJ, Collins MT, Faaberg KS, Wees C, Tavornpanich S, Petrini KR, Collins JE, Cernicchiaro N, Whitlock RH. 2006. Evaluation of a rapid fecal PCR test for detection of Mycobacterium avium subsp. Paratuberculosis in dairy cattle. Clin. Vaccine Immunol. 13:1125-1130. http://dx.doi .org/10.1128/CVI. 00236-06. (Pubitemid 44622540)
43. Nielsen SS, Toft N. 2008. Ante mortem diagnosis of paratuberculosis: a review of accuracies of ELISA, interferon-gamma assay and faecal culture techniques. Vet. Microbiol. 129:217-235. http://dx.doi.org/10.1016/j.vetmic. 2007.12.011.